skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Chromatin organization regulates viral egress dynamics

Journal Article · · Scientific Reports
 [1];  [1];  [2];  [2];  [2];  [3];  [4];  [5]; ORCiD logo [6]; ORCiD logo [7];  [8];  [2]
  1. Univ. of Jyvaskyla (Finland). Dept. of Physics
  2. Univ. of Jyvaskyla (Finland). Dept. of Biological and Environmental Science
  3. Univ. of Helsinki (Finland). Inst. of Biotechnology
  4. Univ. of Turku (Finland). Faculty of Medicine
  5. Univ. of Eastern Finland, Kuopio (Finland). Dept. of Applied Physics; Finnish Meteorological Inst. Kuopio (Finland)
  6. Univ. of Jyvaskyla (Finland). Dept. of Physics; ITMO Univ., St. Petersburg (Russia)
  7. Univ. of Jyvaskyla (Finland). Dept. of Physics; Tampere Univ. of Technology (Finland). Dept. of Physics
  8. Univ. of California, San Francisco, CA (United States). Dept. of Anatomy; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division

Various types of DNA viruses are known to elicit the formation of a large nuclear viral replication compartment and marginalization of the cell chromatin. We used three-dimensional soft x-ray tomography, confocal and electron microscopy, combined with numerical modelling of capsid diffusion to analyse the molecular organization of chromatin in herpes simplex virus 1 infection and its effect on the transport of progeny viral capsids to the nuclear envelope. Our data showed that the formation of the viral replication compartment at late infection resulted in the enrichment of heterochromatin in the nuclear periphery accompanied by the compaction of chromatin. Random walk modelling of herpes simplex virus 1–sized particles in a three-dimensional soft x-ray tomography reconstruction of an infected cell nucleus demonstrated that the peripheral, compacted chromatin restricts viral capsid diffusion, but due to interchromatin channels capsids are able to reach the nuclear envelope, the site of their nuclear egress.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1379889
Journal Information:
Scientific Reports, Vol. 7, Issue 1; ISSN 2045-2322
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 15 works
Citation information provided by
Web of Science

References (46)

The Herpes Simplex Virus Protein pUL31 Escorts Nucleocapsids to Sites of Nuclear Egress, a Process Coordinated by Its N-Terminal Domain journal June 2015
Transcription-associated histone modifications and cryptic transcription journal January 2013
Tomographic imaging of biological specimens with the cryo transmission X-ray microscope journal July 2001
Histone Deacetylases in Herpesvirus Replication and Virus-Stimulated Host Defense journal June 2013
Nuclear Herpesvirus Capsid Motility Is Not Dependent on F-Actin journal October 2014
Intranuclear Localization of Herpes Simplex Virus Immediate-Early and Delayed-Early Proteins: Evidence that ICP 4 Is Associated with Progeny Virus DNA journal October 1986
Polycomb-Dependent H3K27me1 and H3K27me2 Regulate Active Transcription and Enhancer Fidelity journal January 2014
Soft X-ray tomography and cryogenic light microscopy: the cool combination in cellular imaging journal November 2009
Membrane deformation and scission by the HSV-1 nuclear egress complex journal June 2014
Innate and Adaptive Immune Responses to Herpes Simplex Virus journal November 2009
Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo journal November 2016
Chromatin control of herpes simplex virus lytic and latent infection journal March 2008
Chromatin Movement in the Maintenance of Genome Stability journal March 2013
The Influence of Spatial Variation in Chromatin Density Determined by X-Ray Tomograms on the Time to Find DNA Binding Sites journal August 2013
Exploring the Nuclear Envelope of Herpes Simplex Virus 1-Infected Cells by High-Resolution Microscopy journal October 2008
The herpes simplex virus 1 UL41 gene-dependent destabilization of cellular RNAs is selective and may be sequence-specific journal March 2004
Formation of herpes simplex virus type 1 replication compartments by transfection: requirements and localization to nuclear domain 10. journal January 1997
Parvovirus Induced Alterations in Nuclear Architecture and Dynamics journal June 2009
Nucleolin Is Required for an Efficient Herpes Simplex Virus Type 1 Infection journal March 2008
Imaging and characterizing cells using tomography journal September 2015
Structural Basis of Vesicle Formation at the Inner Nuclear Membrane journal December 2015
From The Cover: Histone H3.3 is enriched in covalent modifications associated with active chromatin journal January 2004
Herpesvirus Replication Compartments Originate with Single Incoming Viral Genomes journal December 2011
Continuous-time random walks on random media journal June 1993
Correlative cryogenic tomography of cells using light and soft x-rays journal August 2014
Compensation for Nonuniform Resolution Using Penalized-Likelihood Reconstruction in Space-Variant Imaging Systems journal March 2004
Active genes are tri-methylated at K4 of histone H3 journal September 2002
Remodeling nuclear architecture allows efficient transport of herpesvirus capsids by diffusion journal October 2015
A new algorithm for Monte Carlo simulation of Ising spin systems journal January 1975
Herpes simplex virus 1 induces egress channels through marginalized host chromatin journal June 2016
Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells journal June 2004
Herpes Simplex Virus Triggers and Then Disarms a Host Antiviral Response journal January 2001
X-ray tomography of whole cells journal October 2005
Soft X-ray microscopy analysis of cell volume and hemoglobin content in erythrocytes infected with asexual and sexual stages of Plasmodium falciparum journal February 2012
Annexation of the interchromosomal space during viral infection journal August 2000
Regulation of chromatin by histone modifications journal February 2011
A Single Herpesvirus Protein Can Mediate Vesicle Formation in the Nuclear Envelope journal January 2015
Recruitment of Herpes Simplex Virus Type 1 Transcriptional Regulatory Protein ICP4 into Foci Juxtaposed to ND10 in Live, Infected Cells journal March 2003
A guided tour into subcellular colocalization analysis in light microscopy journal December 2006
Histone modifications in herpesvirus infections journal January 2012
Nuclear Marginalization of Host Cell Chromatin Associated with Expansion of Two Discrete Virus-Induced Subnuclear Compartments during Baculovirus Infection journal April 2008
Herpesviruses carrying a Brainbow cassette reveal replication and expression of limited numbers of incoming genomes journal December 2010
Random Walks on Lattices. II journal February 1965
Herpes Simplex Virus 1 UL31 and UL34 Gene Products Promote the Late Maturation of Viral Replication Compartments to the Nuclear Periphery journal May 2004
Automatic alignment and reconstruction of images for soft X-ray tomography journal February 2012
Modelling diffusion in a heterogeneous rock matrix with a time-domain Lagrangian method and an inversion procedure journal October 2002

Cited By (4)

Venture from the Interior—Herpesvirus pUL31 Escorts Capsids from Nucleoplasmic Replication Compartments to Sites of Primary Envelopment at the Inner Nuclear Membrane journal November 2017
Imaging cell morphology and physiology using X-rays journal April 2019
The protective function of non-coding DNA in DNA damage accumulation with age and its roles in age-related diseases journal August 2019
Cryo-soft X-ray tomography: using soft X-rays to explore the ultrastructure of whole cells journal March 2018